Toxic Cyanobacteria in Water; a Guide to Their Public Health

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Toxic Cyanobacteria in Water; a Guide to Their Public Health Chapter 3 Introduction to cyanobacteria Leticia Vidal, Andreas Ballot, Sandra M. F. O. Azevedo, Judit Padisák and Martin Welker CONTENTS Introduction 163 3.1 Cell types and cell characteristics 164 3.2 Morphology of multicellular forms 168 3.3 Cyanobacterial pigments and colours 170 3.4 Secondary metabolites and cyanotoxins 171 3.5 Taxonomy of cyanobacteria 172 3.6 Major cyanobacterial groups 178 3.7 Description of common toxigenic and bloom-forming cyanobacterial taxa 179 3.7.1 Filamentous forms with heterocytes 190 3.7.2 Filamentous forms without heterocytes and akinetes 195 3.7.3 Colonial forms 200 Picture credits 203 References 204 INTRODUCTION Cyanobacteria are a very diverse group of prokaryotic organisms that thrive in almost every ecosystem on earth. In contrast to other prokaryotes (bacteria and archaea), they perform oxygenic photosynthesis and possess chlorophyll-a. Their closest relatives are purple bacteria (Woese et al., 1990; Cavalier-Smith, 2002) – and chloroplasts in higher plants (Moore et al., 2019). Photosynthetic activity of cyanobacteria is assumed to have changed the earth’s atmosphere in the Proterozoic Era some 2.4 billion years ago during the so-called Great Oxygenation Event (Hamilton et al., 2016; Garcia-Pichel et al., 2019). Historically, cyanobacteria were considered as plants or plant-like organ- isms and were termed “Schizophyceae”, “Cyanophyta”, “Cyanophyceae” or “blue-green algae”. Since their prokaryotic nature has unambiguously been proven, the term “cyanobacteria” (or occasionally “cyanoprokary- otes”) has been adopted in the scientific literature. A metagenomic study by Soo et al. (2017) revealed that cyanobacteria also comprise groups of 163 164 Toxic Cyanobacteria in Water nonphotosynthetic bacteria and the taxon Oxyphotobacteria is proposed for cyanobacteria in a strict sense. However, in this volume, the term “cya- nobacteria” will be used for photosynthetic, oxygenic bacteria. 3.1 CELL TYPES AND CELL CHARACTERISTICS As prokaryotes, cyanobacteria lack a cell nucleus and other cell organelles, allowing their microscopic distinction from most other microalgae. In par- ticular, cyanobacteria lack chloroplasts, and instead, the chlorophyll for the photosynthesis is contained in simple thylakoids, the site of the light- dependent reactions of photosynthesis (exception: Gloeobacter spp. not possessing thylakoids). Cyanobacteria occur as unicellular, colonial or mul- ticellular filamentous forms. Diverse forms populate all possible environ- ments where light and at least some water and nutrients are available – even if only in very low quantities. Examples for extreme environments in which cyanobacteria can be encountered are caves or deserts (Whitton & Potts, 2000). This volume primarily considers cyanobacteria in the aquatic envi- ronments where they may grow suspended in water (i.e., as “plankton”), attached to hard surfaces (“benthos” or “benthic”, respectively), or to mac- rophytes or any other submerged surfaces (“periphytic” or “metaphytic”). Sexual reproduction has not been observed for cyanobacteria; there- fore, their only means of reproduction is asexual, through division of veg- etative cells. The morphology of cyanobacterial cells shows a number of characteristics that can be used for microscopic examination and identification: primar- ily, the shape and size of cells, subcellular structures and specialised cells (Figure 3.1–3.3). Cyanobacterial cells can be spherical, ellipsoid, barrel- shaped, cylindrical, conical or disc-shaped. Some taxa include cells of dif- ferent shapes. Cyanobacteria do not possess flagella, as are found in many other bacterial or phytoplankton taxa. Nevertheless, many cyanobacteria, in particular filamentous forms, show gliding motility, the mechanism of which is not yet fully understood (Hoiczyk, 2000; Read et al., 2007). The size of cyanobacteria varies considerably between taxa: more or less spherical cells of unicellular cyanobacteria range in diameter from about 0.2 μm to over 40 μm. In consequence, cell volume may vary by a factor of at least 300 000, making simple cell counts an unreliable parameter for the determination of biomass, especially when reported without differen- tiation between individual taxa (see Chapter 13). Some filamentous forms have been observed to have cell diameters of up to 100 μm, but as these coin-shaped cells are generally very short, their cell volume is not neces- sarily much larger than that of other species (Figure 3.2; Whitton & Potts, 2000). The length of filaments (or trichomes; see below) can reach a few millimetres in certain benthic forms. Very small cells of cyanobacteria (in the size range 0.2–2 μm) have been recognised as a significant fraction of 3 Introduction to cyanobacteria 165 (a) straight bent curved, flexuous coiled, spiral (b) unsheathed trichome sheathed trichome pseudofilament (c) false branching true branching Figure 3.1 Characteristics of cyanobacteria filaments. (a) General shapes; (b) presence of sheaths; (c) branching types. (a) cylindrical, not constricted cylindrical, slightly constricted barrel shaped, constricted elliptical, constricted spherical (b) cell length << widths cell length ≈ widths cell length >> widths (c) not attenuated terminal cell attenuated slightly attenuated attenuated attenuated and elongated Figure 3.2 Characteristics of cyanobacteria filaments. (a) Cell shapes and arrangement in filaments; (b) cell length-to-width ratios; (c) filament terminal region. 166 Toxic Cyanobacteria in Water (a) (sub)symmetric subterminal terminal intercalary serial (b) (sub)symmetric serial paraheterocytic solitary, separated Figure 3.3 A rrangement of heterocytes (a) and akinetes (b) in filamentous cyanobacteria. the so-called picoplankton in various freshwater and marine environments, such as Prochlorococcus that is found in huge numbers in the world’s oceans (Flombaum et al., 2013). The occurrence of picocyanobacteria in freshwaters is well established (Postius & Ernst, 1999; Stomp et al., 2007) but possibly is underestimated, especially when biomass estimates are based on microscopy. With molecular tools such as metagenomics (section 13.4), our understanding of the role of picocyanobacteria in lake ecosystems may increase (Śliwińska-Wilczewska et al., 2018; Nakayama et al., 2019). A number of cyanobacterial taxa can (facultatively) produce so-called aerotopes that are clearly visible in microscopy as light-refracting struc- tures. Aerotopes (sometimes incorrectly named “gas vacuoles” – they are not vacuoles in the cytological sense) are bundles of cylindrical protein microstructures that form the gas vesicles. These vesicles are filled with air entering the lumen by diffusion (see Walsby (1994) for an extensive review). Gas vesicles have a density of about one-tenth of that of water and thus render the entire cells less dense than water, providing buoyancy and making them float or emerge to the water surface (see Section 3.2). The gas vesicles measure some 75 nm in diameter and up to 1.0 μm in length. The cylinders, capped by conical ends, are formed by a single wall layer of 2 nm thickness. The distribution of aerotopes within the cells is character- istic for individual taxa and can be used for identification by microscopical examination, but they can disintegrate after fixation with Lugol’s solution (see Chapter 13). Other subcellular (ultrastructural) characteristics such as the distribu- tion of thylakoids are used in taxonomic studies (Hoffmann et al., 2005; Komárek et al., 2014). As thylakoids are not visible using light microscopy with standard equipment, other methodologies are generally applied for their examination, such as transmission electron microscopy. In some groups of cyanobacteria (see Table 3.1), specialised cells occur, which are morphologically different from vegetative cells and which can be 3 Introduction to cyanobacteria 167 Table 3.1 Major groups of cyanobacteria in the taxonomic schemes proposed by Castenholz et al. (2001) and Cavalier-Smith (2002) Group Morphological characteristics Genera (selection) Subsection 1 • Unicellular Aphanocapsa, “Chroococcales” • Colonies with regular or irregular Gomphospheria, cell arrangement Merismopedia, Microcystis, • Embedded in extracellular mucilage Synechococcus, Synechocystis, Woronichinia Subsection 2 • Colonial or filamentous Pleurocapsa, “Pleurocapsales” • Reproduction through baeocytes Chroococcidiopsis, Cyanocystis Subsection 3 • Multiplication by hormogonia Leptolyngbya, Lyngbya, “Oscillatoriales” • Unbranched, linear filaments Microcoleus, Oscillatoria, • No heterocytes or akinetes Phormidium, Planktothrix, • Cells typically shorter than broad Pseudanabaena, Tychonema Subsection 4 • Multiplication by hormogonia Anabaena, Aphanizomenon, “Nostocales” • Nonbranching or false branching Raphidiopsis • Heterocytes (can be absent in (Cylindrospermopsis), individual filaments) Cuspidothrix, Chrysosporum, • Akinetes Dolichospermum, Nostoc, Sphaerospermopsis Subsection 5 • Multiplication by hormogonia Chlorogloeopsis, Fischerella, “Stigonematales” • True branching Stigonema • Heterocytes (can be absent in individual filaments) • Akinetes The morphological characteristics are based on microscopic observation. Exemplary genera are given for subsections. generally easily recognised by light microscopy (see examples below), that is, heterocytes and akinetes. Heterocytes are specialised cells that allow the fixation of atmospheric nitrogen, a process also called diazotrophy that involves nitrogenases, enzymes capable to
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